An Envelope-determined Endocytic Route of Viral Entry Allows HIV-1 to Escape from Secreted Phospholipase A2 Entry Blockade

Journal of Molecular Biology

Volumn 367, Issue 3, 2007, Pages 702-714

  Maurin, Thomas ^a   Fenard, David ^a   Lambeau, Gérard ^b   Doglio, Alain ^a  

^a INSERM   (France)

^b INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

endosomal trafficking; entry inhibitors; HIV 1 entry; HIV 1 envelope protein; sPLA2

Indexed keywords

BAFILOMYCIN A1; GLYCOPROTEIN; LATRUNCULIN A; MONENSIN; NOCODAZOLE; PHOSPHOLIPASE A2; VIRUS PROTEIN;

ACIDIFICATION; AMINO TERMINAL SEQUENCE; ARTICLE; CELL MIGRATION; CHIMERA; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; ENZYME RELEASE; GENE MUTATION; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; VIRUS ENVELOPE; VIRUS ISOLATION; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 33847405642     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.01.031     Document Type: Article

References (71)

1. Lambeau G., and Lazdunski M. Receptors for a growing family of secreted phospholipases A2. Trends Pharmacol. Sci. 20 (1999) 162-170
2. Dennis E.A. The growing phospholipase A2 superfamily of signal transduction enzymes. Trends Biochem. Sci. 22 (1997) 1-2
3. Murakami M. Hot topics in phospholipase A2 field. Biol. Pharm. Bull. 27 (2004) 1179-1182
4. Balsinde J., Winstead M.V., and Dennis E.A. Phospholipase A(2) regulation of arachidonic acid mobilization. FEBS Letters 531 (2002) 2-6
5. Kini R.M., and Evans H.J. A model to explain the pharmacological effects of snake venom phospholipases A2. Toxicon 27 (1989) 613-635
6. Murakami M., Nakatani Y., Atsumi G., Inoue K., and Kudo I. Regulatory functions of phospholipase A2. Crit. Rev. Immunol. 17 (1997) 225-283
7. Lambeau G., Cupillard L., and Lazdunski M. Membrane receptors for venom phospholipases A2. In: Kini R.M. (Ed). Venom Phospholipase A2 Enzymes: Structure, Function and Mechanism (1997), Wiley & Sons, J., Chichester 389-412
8. Vadas P., Browning J., Edelson J., and Pruzanski W. Extracellular phospholipase A2 expression and inflammation: the relationship with associated disease states. J. Lip. Med. 8 (1993) 1-30
9. MacPhee M., Chepenik K.P., Liddell R.A., Nelson K.K., Siracusa L.D., and Buchberg A.M. The secretory phospholipase A2 gene is a candidate for the Mom1 locus, a major modifier of ApcMin-induced intestinal neoplasia. Cell 81 (1995) 957-966
10. Rouault M., Bollinger J.G., Lazdunski M., Gelb M.H., and Lambeau G. Novel mammalian group XII secreted phospholipase A2 lacking enzymatic activity. Biochemistry 42 (2003) 11494-11503
11. Murakami M., and Kudo I. Secretory phospholipase A2. Biol. Pharm. Bull. 27 (2004) 1158-1164
12. Gronroos J.O., Laine V.J., and Nevalainen T.J. Bactericidal group IIA phospholipase A2 in serum of patients with bacterial infections. J. Infect. Dis. 85 (2002) 1767-1772
13. Guillaume C., Deregnaucourt C., Clavey V., and Schrevel J. Anti-Plasmodium properties of group IA, IB, IIA and III secreted phospholipases A2 are serumdependent. Toxicon 43 (2004) 311-318
14. Koduri R.S., Gronroos J.O., Laine V.J., Le Calvez C., Lambeau G., Nevalainen T.J., and Gelb M.H. Bactericidal properties of human and murine groups I, II, V, X, and XII secreted phospholipases A(2). J. Biol. Chem. 277 (2002) 5849-5857
15. Weinrauch Y., Elsbach P., Madsen L.M., Foreman A., and Weiss J. The potent anti-Staphylococcus aureus activity of a sterile rabbit inflammatory fluid is due to a 14-kDa phospholipase A2. J. Clin. Invest. 97 (1996) 250-257
16. Fenard D., Lambeau G., Maurin T., Lefebvre J.C., and Doglio A. A peptide derived from bee venom-secreted phospholipase A2 inhibits replication of T-cell tropic HIV-1 strains via interaction with the CXCR4 chemokine receptor. Mol. Pharmacol. 60 (2001) 341-347
17. Fenard D., Lambeau G., Valentin E., Lefebvre J.C., Lazdunski M., and Doglio A. Secreted phospholipases A(2), a new class of HIV inhibitors that block virus entry into host cells. J. Clin. Invest. 104 (1999) 611-618
18. Kini R.M. The intriguing world of prothrombin activators from snake venom. Toxicon 45 (2005) 1133-1145
19. Valentin E., and Lambeau G. What can venom phospholipases A(2) tell us about the functional diversity of mammalian secreted phospholipases A(2)?. Biochimie 82 (2000) 815-831
20. Chan D.C., and Kim P.S. HIV entry and its inhibition. Cell 93 (1998) 681-684
21. Colman P.M., and Lawrence M.C. The structural biology of type I viralmembrane fusion. Nature Rev. Mol. Cell. Biol. 4 (2003) 309-319
22. Sieczkarski S.B., and Whittaker G.R. Dissecting virus entry via endocytosis. J. Gen. Virol. 83 (2002) 1535-1545
23. Whittaker G.R., Kann M., and Helenius A. Viral entry into the nucleus. Annu. Rev. Cell. Dev. Biol. 16 (2000) 627-651
24. Pelkmans L., Kartenbeck J., and Helenius A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nature Cell. Biol. 3 (2001) 473-483
25. Fackler O.T., and Peterlin B.M. Endocytic entry of HIV-1. Curr. Biol. 10 (2000) 1005-1008
26. Nakai M., and Goto T. Ultrastructure and morphogenesis of human immunodeficiency virus. J. Electron. Microsc. (Tokyo) 45 (1996) 247-257
27. Daecke J., Fackler O.T., Dittmar M.T., and Krausslich H.G. Involvement of clathrin-mediated endocytosis in human immunodeficiency virus type 1 entry. J. Virol. 79 (2005) 1581-1594
28. Vidricaire G., Tardif M.R., and Tremblay M.J. The low viral production in trophoblastic cells is due to a high endocytic internalization of the human immunodeficiency virus type 1 and can be overcome by the pro-inflammatory cytokines tumor necrosis factor-alpha and interleukin-1. J. Biol. Chem. 278 (2003) 15832-15841
29. Marechal V., Prevost M.C., Petit C., Perret E., Heard J.M., and Schwartz O. Human immunodeficiency virus type 1 entry into macrophages mediated by macropinocytosis. J. Virol. 75 (2001) 11166-11177
30. Marechal V., Clavel F., Heard J.M., and Schwartz O. Cytosolic Gag p24 as an index of productive entry of human immunodeficiency virus type 1. J. Virol. 72 (1998) 2208-2212
31. Marchant D., Neil S.J., Aubin K., Schmitz C., and McKnight A. An envelope-determined, pH-independent endocytic route of viral entry determines the susceptibility of human immunodeficiency virus type 1 (HIV-1) and HIV-2 to Lv2 restriction. J. Virol. 79 (2005) 9410-9418
32. Vidricaire G., Imbeault M., and Tremblay M.J. Endocytic host cell machinery plays a dominant role in intracellular trafficking of incoming human immunodeficiency virus type 1 in human placental trophoblasts. J. Virol. 78 (2004) 1904-11915
33. Schaeffer E., Soros V.B., and Greene W.C. Compensatory link between fusion and endocytosis of human immunodeficiency virus type 1 in human CD4 T lymphocytes. J. Virol. 78 (2004) 1375-1383
34. Wei B.L., Denton P.W., O'Neill E., Luo T., Foster J.L., and Garcia J.V. Inhibition of lysosome and proteasome function enhances human immunodeficiency virus type 1 infection. J. Virol. 79 (2005) 5705-5712
35. Fredericksen B.L., Wei B.L., Yao J., Luo T., and Garcia J.V. Inhibition of endosomal/lysosomal degradation increases the infectivity of human immunodeficiency virus. J. Virol. 76 (2002) 11440-11446
36. Nobile C., Petit C., Moris A., Skrabal K., Abastado J.P., Mammano F., and Schwartz O. Covert human immunodeficiency virus replication in dendritic cells and in DC-SIGN-expressing cells promotes long-term transmission to lymphocytes. J. Virol. 79 (2005) 5386-5399
37. Kaushik R., and Ratner L. Role of human immunodeficiency virus type 1 matrix phosphorylation in an early postentry step of virus replication. J. Virol. 78 (2004) 2319-2326
38. Kiernan R.E., Ono A., Englund G., and Freed E.O. Role of matrix in an early postentry step in the human immunodeficiency virus type 1 life cycle. J. Virol. 72 (1998) 4116-4126
39. Fouchier R.A., Meyer B.E., Simon J.H., Fischer U., and Malim M.H. HIV-1 infection of non-dividing cells: evidence that the amino-terminal basic region of the viral matrix protein is important for Gag processing but not for post-entry nuclear import. EMBO J. 16 (1997) 4531-4539
40. Beer C., Andersen D.S., Rojek A., and Pedersen L. Caveola-dependent endocytic entry of amphotropic murine leukemia virus. J. Virol. 79 (2005) 10776-10787
41. Sun X., Yau V.K., Briggs B.J., and Whittaker G.R. Role of clathrinmediated endocytosis during vesicular stomatitis virus entry into host cells. Virology 20 (2005) 53-60
42. Butler S.L., Hansen M.S., and Bushman F.D. A quantitative assay for HIV DNA integration in vivo. Nature Med. 7 (2001) 631-634
43. Bayer N., Schober D., Prchla E., Murphy R.F., Blaas D., and Fuchs R. Effect of bafilomycin A1 and nocodazole on endocytic transport in HeLa cells: implications for viral uncoating and infection. J. Virol. 72 (1998) 9645-9655
44. Yonezawa A., Cavrois M., and Greene W.C. Studies of ebola virus glycoprotein-mediated entry and fusion by using pseudotyped human immunodeficiency virus type 1 virions: involvement of cytoskeletal proteins and enhancement by tumor necrosis factor alpha. J. Virol. 79 (2005) 918-926
45. Asaoka Y., Yoshida K., Sasaki Y., and Nishizuka Y. Potential role of phospholipase A2 in HL-60 cell differentiation to macrophages induced by protein kinase C activation. Proc. Natl Acad. Sci. USA 90 (1993) 4917-4921
46. Urasaki T., Takasaki J., Nagasawa T., and Ninomiya H. Induction of the activation-related antigen CD69 on human eosinophils by type IIA phospholipase A2. Inflamm. Res. 49 (2000) 177-183
47. Rigoni M., Schiavo G., Weston A.E., Caccin P., Allegrini F., Pennuto M., et al. Snake presynaptic neurotoxins with phospholipase A2 activity induce punctate swellings of neurites and exocytosis of synaptic vesicles. J. Cell. Sci. 117 (2004) 3561-3570
48. Neco P., Rossetto O., Gil A., Montecucco C., and Gutierrez L.M. Taipoxin induces F-actin fragmentation and enhances release of catecholamines in bovine chromaffin cells. J. Neurochem. 85 (2003) 329-337
49. Kudo I., and Murakami M. Phospholipase A2 enzymes. Prostaglandins Other Lipid Mediat. 68-69 (2002) 3-58
50. Mothes W., Boerger A.L., Narayan S., Cunningham J.M., and Young J.A. Retroviral entry mediated by receptor priming and low pH triggering of an envelope glycoprotein. Cell 103 (2000) 679-689
51. Picard-Maureau M., Jarmy G., Berg A., Rethwilm A., and Lindemann D. Foamy virus envelope glycoprotein-mediated entry involves a pH-dependent fusion process. J. Virol. 77 (2003) 4722-4730
52. Kuhn M. The microtubule depolymerizing drugs nocodazole and colchicine inhibit the uptake of Listeria monocytogenes by P388D1 macrophages. FEMS Microbiol. Letters 160 (1998) 87-90
53. Hamm-Alvarez S.F., Sonee M., Loran-Goss K., and Shen W.C. Paclitaxel and nocodazole differentially alter endocytosis in cultured cells. Pharm. Res. 13 (1996) 1647-1656
54. Geada M.M., Galindo I., Lorenzo M.M., Perdiguero B., and Blasco R. Movements of vaccinia virus intracellular enveloped virions with GFP tagged to the F13L envelope protein. J. Gen. Virol. 82 (2001) 2747-2760
55. Kizhatil K., and Albritton L.M. Requirements for different components of the host cell cytoskeleton distinguish ecotropic murine leukemia virus entry via endocytosis from entry via surface fusion. J. Virol. 71 (1997) 7145-7156
56. Stuart A.D., Eustace H.E., McKee T.A., and Brown T.D. A novel cell entry pathway for a DAF-using human enterovirus is dependent on lipid rafts. J. Virol. 76 (2002) 9307-9322
57. Merrifield C.J., Perrais D., and Zenisek D. Coupling between clathrin-coatedpit invagination, cortactin recruitment, and membrane scission bserved in live cells. Cell 121 (2005) 593-606
58. Sauvonnet N., Dujeancourt A., and Dautry-Varsat A. Cortactin and dynamin are required for the clathrin-independent endocytosis of gammac cytokine receptor. J. Cell. Biol. 168 (2005) 155-163
59. McDonald D., Vodicka M.A., Lucero G., Svitkina T.M., Borisy G.G., Emerman M., and Hope T.J. Visualization of the intracellular behavior of HIV in living cells. J. Cell. Biol. 159 (2002) 441-452
60. Kwong P.D., Wyatt R., Robinson J., Sweet R.W., Sodroski J., and Hendrickson W.A. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393 (1998) 648-659
61. Walter B.L., Wehrly K., Swanstrom R., Platt E., Kabat D., and Chesebro B. Role of low CD4 levels in the influence of human immunodeficiency virus type 1 envelope V1 and V2 regions on entry and spread in macrophages. J. Virol. 79 (2005) 4828-4837
62. Pugach P., Kuhmann S.E., Taylor J., Marozsan A.J., Snyder A., Ketas T., et al. The prolonged culture of human immunodeficiency virus type 1 in primary lymphocytes increases its sensitivity to neutralization by soluble CD4. Virology 321 (2004) 8-22
63. Chen B., Vogan E.M., Gong H., Skehel J.J., Wiley D.C., and Harrison S.C. Structure of an unliganded simian immunodeficiency virus gp120 core. Nature 433 (2005) 834-841
64. Sagar M., Wu X., Lee S., and Overbaugh J. Human immunodeficiency virus type 1 V1-V2 envelope loop sequences expand and add glycosylation sites over the course of infection, and these modifications affect antibody neutralization sensitivity. J. Virol. 80 (2006) 9586-9598
65. Masciotra S., Owen S.M., Rudolph D., Yang C., Wang B., Saksena N., et al. Temporal relationship between V1V2 variation, macrophage replication, and coreceptor adaptation during HIV-1 disease progression. Aids 16 (2002) 1887-1898
66. Wang B., Spira T.J., Owen S., Lal R.B., and Saksena N.K. HIV-1 strains from a cohort of American subjects reveal the presence of a V2 region extension unique to slow progressors and non-progressors. Aids 14 (2000) 213-223
67. Shioda T., Oka S., Xin X., Liu H., Harukuni R., Kurotani A., et al. In vivo sequence variability of human immunodeficiency virus type 1 envelope gp120: association of V2 extension with slow disease progression. J. Virol. 71 (1997) 4871-4881
68. Lambeau G., Barhanin J., Schweitz H., Qar J., and Lazdunski M. Identification and properties of very high affinity brain membrane-binding sites for a neurotoxic phospholipase from the taipan venom. J. Biol. Chem. 264 (1989) 11503-11510
69. Charneau P., Mirambeau G., Roux P., Paulous S., Buc H., and Clavel F. HIV-1 reverse transcription. A termination step at the center of the genome. J. Mol. Biol. 241 (1994) 651-662
70. Desmezieres E., Gupta N., Vassell R., He Y., Peden K., Sirota L., et al. Human immunodeficiency virus (HIV) gp41 escape mutants: cross-resistance to peptide inhibitors of HIV fusion and altered receptor activation of gp120. J. Virol. 79 (2005) 4774-4781
71. Julenius K., Molgaard A., Gupta R., and Brunak S. Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 15 (2005) 153-164